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Wire Mesh Allows More Revascularization Than a Strut in Impaction Bone Grafting: An Animal Study in Goats

Bolder, Stefan, B. T; Schreurs, B, Willem; Verdonschot, Nico; Veth, Rene, P. H; Buma, Pieter

Clinical Orthopaedics and Related Research: June 2004 - Volume 423 - Issue - p 280-286
doi: 10.1097/01.blo.0000130207.09978.8c

Segmental defects can be reconstructed with a cortical strut or a metal wire mesh when using bone impaction grafting in the femur. We hypothesized that structural grafts would negatively influence revascularization of the underlying impacted grafts compared with an open wire mesh. A standardized large medial wall defect was reconstructed with a strut or a mesh in six goats per group. In all femurs impaction grafting was done in combination with a cemented collarless double-tapered highly polished Exeter stem. After 6 weeks the femurs were harvested. A high rate of periprosthetic fractures was observed (three of seven and two of six for the strut and mesh groups, respectively). Histologic analysis showed different revascularization and tissue ingrowth patterns for both reconstruction techniques. In the strut group, fibrous tissue ingrowth was limited to the edges of the defect. Medially behind the strut no or limited fibrous tissue ingrowth was found. In the mesh group, fibrous tissue and blood vessels penetrated the mesh and a superficial zone of revascularized grafts was observed. Although revascularization, concomitant graft resorption and bone incorporation may compromise the short-term stability of the stem after surgery, the long-term stability of the stem probably is best guaranteed by graft incorporation.

From the Orthopaedic Research Lab, Department of Orthopaedics, University Medical Center Nijmegen, Nijmegen, The Netherlands.

Received: May 5, 2003

Revised: October 6, 2003; January 23, 2004

Accepted: February 24, 2004

This study was sponsored by Stryker Howmedica Osteonics, Newbury, England, and a grant was received from ‘De Drie Lichten’ Foundation, Hilversum, The Netherlands.

Correspondence to: B. W. Schreurs, MD, PhD, Department of Orthopaedics, University Medical Centre Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands. Phone: 31-24 3613918; Fax: 31-24 3540230; E-mail:

In complex primary and revision hip surgery, bone stock deficiencies frequently are encountered. Several reconstruction techniques have been suggested, including the bone impaction grafting technique advocated by Slooff et al29 and Gie et al.8 The aim of this technique is to obtain stable implant fixation, to restore normal hip biomechanics, and in the long-term, a normal revitalized bone with an original anatomy.

Clinical results have been satisfying on the acetabular2,21,28,34 and femoral6,8,12,15,32 sides. However, some authors have reported a high incidence of complications, particularly on the femoral side, and especially when the technique is used in combination with segmental defects.4,5,13,18,19,23 Most reported complications are high subsidence rates and periprosthetic fractures. Originally, in patients with a deficient cortical wall, the bone impaction grafting technique was used in combination with metal meshes.9 Another option is to reconstruct segmental defects with a cortical strut graft.7,10 Bolder et al3 showed, in an in vitro goat study, that segmental defect repair is required for adequate initial stem stability. In combination with bone impaction grafting, cortical struts and metal meshes were equally effective in creating a stable stem construction, although the obtained stability was inferior relative to bone impaction grafting in an intact femur.3

Few studies are available on the incorporation of femoral bone impaction grafting under struts or meshes.14,16 In general, blood vessels and fibrous tissue from the host invade the impacted grafts layer in the first weeks after surgery11,14,16,17,25,27,30,33 to ensure sufficient host parameters for graft incorporation. Mechanically, reconstructions with a strut showed more variability.3 However, from a biologic view, struts seem to be a more attractive option in the treatment of segmental defects of the femur than meshes, as struts also can be revascularized in vivo and may incorporate in the long term.7,10 It is unknown to what extent the presence of a structural graft may interfere with revascularization of the underlying impacted grafts in comparison with an open wire mesh when used in combination with bone impaction grafting.

We hypothesized that the strut graft technique used for reconstruction of a medial segmental defect in the femur will decrease the ingrowth of host tissue into the impacted graft under the reconstruction.

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Based on earlier experience,27 femoral reconstructions were done in adult Dutch milk goats (Capra Hircus Sana). The same critical-sized medial wall defect as used in the biomechanical in vitro study3 was used in vivo. Femoral reconstructions with impaction bone grafting were done in 12 goats (range, 55–76 kg). In six goats, the segmental defect was reconstructed with a cortical strut. In six goats, a metal mesh was used to contain the defect. The ethical committee of our institution approved the study.

Pure cancellous bone grafts were obtained from the sternum of donor goats under sterile conditions. To improve the reproducibility, a pool of bone grafts was made from several donor goats. Strut grafts were obtained from the proximal femur of the donor goats. After harvesting, the bone grafts and the cortical struts were stored at –80°C until use. Bacterial cultures of the cancellous bone grafts and the cortical struts were taken.

Femoral reconstructions were done similar to earlier goat studies.3,27 The goats were anesthetized while lying on their left side. The right hip was shaved and sterilized with an ethanol-iodide solution. Through a posterolateral approach the hip was exposed. The hip was dislocated and the femoral head was removed. The femoral shaft was cleared using a special set of instruments for the goat, similar to the Howmedica X-Change Revision set (Stryker Howmedica Osteonics, Newbury, United Kingdom). This set was used in earlier experiments to develop the X-Change femoral system.27 Two femoral broaches were available. The femoral canal was lavaged and the cement plug was measured. The bone restrictor (X-Change Revision plug) was inserted. The central rod of the femoral impaction system was attached to the plug and was used as a guide (Fig 1). The femur was filled with impacted morselized bone grafts up to the most distal level of the segmental defect before creating the medial wall defect. A standardized medial segmental defect was made using a template after the distal impaction (Fig 2). The defect was similar to the defect in the biomechanical study3 and was categorized as a Type 2C femoral defect by the classification of Pak et al22 with extensive posteromedial subtrochanteric metaphyseal bone loss. The defect extended 4.5 cm distally from the resection level and had a width of 2 cm. The segmental defect was reconstructed with a strut graft or a metal mesh, which was fixed with three cerclage wires (diameter, 1 mm). In all goats, the cerclage wires were applied at the same level. We aimed to let the strut and mesh overlie the defect for 5–7 mm on both sides. After segmental defect reconstruction, the proximal femur was filled with impacted cancellous bone chips. Several impactors were available including a stem phantom to impact the grafts axially and radially. Bone cement (Surgical Simplex, Stryker Howmedica Osteonics) was injected retrogradely 3.5 minutes after adding the powder to the monomer, followed by inserting the collarless double-tapered polished Exeter sheep stem with a centralizer 5 minutes after mixing. The stem used in this study was specially made for use in animal experiments.

Fig 1.

Fig 1.

Fig 2.

Fig 2.

Postoperative treatment included nonweightbearing care in a hammock for as much as 1 week. After 1 week, full weightbearing was allowed in a separate cage. Clinical followup was assessed daily. The goats were euthanized after 6 weeks. The goats received intravital fluorochromes (calcein-green, 20 mg/kg) on Days 35 and 41.

All goats received heparin 200 U/kg intravenously to prevent clotting of the blood before euthanasia. All goats were euthanized with an overdose of pentobarbital (Ceva sante, Animal BV, Maassluis, The Netherlands). Lower body perfusion with barium sulfate (Micropaque Suspension, Codali Guerbet, Brussels, Belgium) was done to analyze revascularization in the graft with microangiography.24 The descending aorta and the vena cava inferior were cannulated and the lower body was perfused with 1 L of 30% barium sulfate in saline, followed by perfusing the lower body with 1 L of 15% barium sulfate in a phosphate-buffered solution of 4% paraformaldehyde. After perfusion of the lower body, femurs and surrounding soft tissue were harvested by careful exarticulation in the hip and knee and stored in a 70/30 mixture of ethanol 96% and 4% buffered paraformaldehyde solution for 24 hours. After 24 hours, excess soft tissue was removed and fixation was continued in a 4%-buffered paraformaldehyde solution.

All femurs were serially sectioned with thin carbon blades on a water-cooled saw (Wolfgang Conrad Fine Mechaniek, Clausthal Zellerfeld, Germany) in 2-mm slices. Three levels were examined in detail: a proximal level, 2–6 mm distal of the proximal edge of the mesh, a level 2–6 mm proximal of the distal edge of the defect, and a level 2–6 mm distal to the tip of the prosthesis. Sawing was done with the stem in situ. At each level, three consecutive slices were taken for routine histologic analysis, fluorescence microscopy, and microangiography, respectively. After making contact radiographs, the wire mesh and the stem were removed in slices for routine histologic analysis. After decalcification in 25% EDTA, the slices were embedded in PMMA. During this process, the bone cement was dissolved. Sections of 7 μm were stained with hematoxylin and eosin. All sections were examined by two authors (SBTB, PB). A consensus opinion was made on the boundary of the fibrous tissue ingrowth into the graft. For fluorescence microscopy, the slices were dehydrated with graded ethanol. Slices were embedded in Epon 812 (Merck KgaA, Darmstadt, Germany) and sawing sections of 30 μm were made. Slices for microangiography were decalcified with 5% formic acid. Microradiograms of the 2-mm slices were taken with an xray diffraction spectrophotometer (Philips PW 1120, Philips, Eindhoven, The Netherlands).

Histomorphometric examination was done with analySIS Software, version 3.2 (Soft Imaging System GmbH, Münster, Germany). The total graft area (in mm2) beneath the strut or mesh was scored in the proximal histologic sections. The hematoxylin and eosin-stained sections were used for quantitation of areas with fibrous tissue ingrowth in the graft (in mm2). The percentage of revascularized graft was calculated by dividing areas with fibrous tissue by the total graft area beneath the strut or mesh. A similar procedure was done for the medial third part of the impacted graft behind the strut or mesh to reduce the effect of revascularization of the graft by the host femur at the edges of the defect. Statistical analysis was done using the Mann-Whitney test.

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Fourteen goats were scheduled for surgery. In each group one goat was excluded because of early death. Each was replaced. In the group with segmental defect reconstruction with a metal mesh, one goat died on the third postoperative day from massive pulmonary infection. We decided to replace this goat because its death was not related to the surgical variable. However, the newly included goat could not be operated on because of foot and mouth disease with prohibition of animal transport, leaving only five goats in the mesh group. In the group with segmental defect reconstruction with a cortical strut, one goat had a periprosthetic fracture after trauma when leaving the cage and the goat was euthanized 5 days after surgery. This goat was replaced.

In each group, the main complication observed during clinical followup was a periprosthetic fracture at the tip of the prosthesis. In the mesh reconstruction group, four of the five goats started full weightbearing 7–10 days after surgery. One of the goats had a dropping foot postoperatively because of sciatic nerve stretching, but was able to walk with partial weightbearing on the right foot. The goats had a slight (three goats), moderate (one goat), or severe (one goat) limp. In two goats the limp was progressive after 4 weeks. At euthanasia both goats with a progressive limp had a periprosthetic femoral fracture with massive callus formation. In the strut reconstruction group one goat fell on the tenth postoperative day, but started partial weightbearing after the fall. There were no clinical signs of fracture except for partial weightbearing and this goat was included. Four goats started full weightbearing 7–11 days after surgery. Two goats were able to walk with partial weightbearing. The goats had no (one goat), slight (three goats), moderate (one goat), or severe (one goat) limp. In one goat the limp was progressive during the last week. In the goat with the progressive limp and in the goat that fell, periprosthetic fractures were seen at euthanasia.

Macroscopic observation of the contact radiographs of the bone slabs showed an impacted graft layer of at least 4-mm thickness behind the strut and the mesh. The fractured femurs showed a high amount of callus formation. Consolidation of the fractures was seen in all fractured femurs. The prosthesis was well positioned in all femurs with a thin cement mantle on the lateral side. The femoral canal was filled with various amounts of bone cement in the distal slices.

Histologic analysis showed that fibrous tissue ingrowth in the impacted graft layer was decreased in the strut graft reconstruction. Sections from the proximal level showed necrotic graft remnants and various amounts of fibrous ingrowth under the struts and meshes. Differences between vital revascularized fibrous tissue and necrotic graft and fibrin remnants were clearly visible in sections stained with hematoxylin and eosin. The transition between these two tissue types was rather sharp. In the reconstructions with the metal mesh a superficial zone of ingrowth was visible throughout the impacted grafts layer (Fig 3). In the reconstructions with a strut, fibrous ingrowth from the host occurred only from the edges of the defect, probably using the gap between strut and host bone (Fig 4). Medially no fibrous ingrowth was seen and only necrotic graft remnants were visible. Sections from the middle level showed a smaller amount of impacted grafts, which were invaded by fibrous tissue. Sections from the distal level showed a various amount of necrotic, nonrevascularized graft remnants. Irrespective of the location, fibrous ingrowth never reached the bone-cement interface in both groups. Fluorescence microscopy showed no signs of new bone formation after 6 weeks behind the strut or mesh in the medial defect. Beginning new bone formation only was seen in the impacted graft with direct contact with the host femur on the mediolateral and posterolateral sides.

Fig 3.

Fig 3.

Fig 4.

Fig 4.

The extent of necrosis of the cortical bone varied, depending on the location, but was not dependent on reconstruction with strut or mesh. The inner 50% endosteal part of the cortical wall was always necrotic. Proximally, near the defect site the cortical bone was almost completely necrotic and reduced periosteal repair of the host cortical bone was seen in most cases. At all other locations a hypertrophic periosteal reaction was observed. All goats with a femoral fracture had enormous periosteal callous repair in these sections with a large amount of fibrous ingrowth in the impacted grafts. In all reconstructions with a strut, a bony bridge from the host femur to the strut was seen, particularly in the sections from the middle level. No signs of revascularization, incorporation, or bone apposition on the struts were observed.

Microangiography showed a perfusion pattern of the impacted grafts that overlapped the area of fibrous tissue ingrowth as was observed in the hematoxylin and eosin-stained sections. Host blood vessels penetrated the graft from the edges, around the strut graft in the femurs with segmental defect reconstruction with a strut. On the edges of the defect revascularized graft was observed. Blood vessels penetrated through the open wire mesh from the soft tissue in the reconstructions with a metal mesh. A superficial zone of revascularized impacted grafts was observed. In both groups, the blood vessels did not penetrate the entire graft and the bone grafts near to the cement remained nonvascularized.

Histomorphometric examination showed that the percentage of new vital tissue ingrowth in the goats with segmental defect reconstruction with a cortical strut was smaller than the goats with segmental defect reconstruction with a metal mesh (Table 1). This difference was not significant (p = 0.13) when the percentage of revascularized graft was calculated as a percentage of the total graft. This difference was significant (p = 0.004) in the medial third, where tissue ingrowth from the host femur was minimal.

Table 1

Table 1

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Several authors have reported a high incidence of complications with impaction grafting on the femoral side,4,5,13,18,19,23 especially when the technique is used in combination with segmental defects. Clinical results in femoral impaction grafting depend on surgical, mechanical, and histologic factors. Firm impaction of cancellous allografts should provide adequate initial stability of the implant.12,21 The presence of a segmental defect significantly decreased initial stem stability on the femoral side.3

The segmental defects were reconstructed with a strut graft or a metal mesh. In vitro, struts and meshes were equally effective in creating a stable stem reconstruction in combination with impaction grafting in the femur.3 The effect of segmental defect reconstruction on the revascularization of the impacted bone grafts under the reconstruction is unknown. Ingrowth of blood vessels and fibrous tissue from the host is required for bony healing in the long term. We hypothesized that the presence of a structural graft might decrease the ingrowth of host tissue into the impacted graft in contrast to an open wire mesh.

Incorporation of morselized bone grafts can be divided into an early phase of new bone formation and a late phase of remodeling.33 The current study focused on the early phase of incorporation in a deficient goat femur model and only one time was measured. The true long-term outcome can be determined only in a study with a longer followup. We only did reconstructions with a medial defect in the calcar region of the femur. No segmental defects on the lateral side of the femur were done in this study. Growth factors are important in the early phase of incorporation, but were not measured in this study.

One of the philosophies of bone impaction grafting includes the incorporation of impacted bone grafts in the long term. In contrast to animal studies25,27 and human retrievals on the acetabular side,11,33 long-term femoral incorporation has been reported as incomplete in humans,14,16,20,31 even in well-functioning patients.14 Under the metal mesh, the cortical wall regenerated. Beneath the cortical bone, viable bone and fibrous tissue were seen in an interface zone. Necrotic graft remnants were present near the bone cement years after surgery. Most retrievals were from older patients with a deficient femur and a mesh reconstruction, which may partially explain the incomplete incorporation.14,16,20

Our results from this study indicate that new bone formation is reduced in femurs with a segmental defect in comparison with a previous goat study with an intact femur.27 No new bone formation was observed in either group in our study. Impaction grafting in an intact femur did result in new bone formation proximally after 6 weeks followup in an in vivo goat study.27 Results from our pilot study with a followup of 12 weeks in two goats with the same defect and reconstructed with a mesh indicated that progression of the ingrowth zone in at least the mesh group can be expected. However, in contrast to 12 week-results in an intact femur, a large amount of graft resorption was observed with minimal new bone formation. Bone graft incorporation in a deficient femur with impaired vascularity seemed to be a different biologic process than impaction grafting in an intact femur. Intramedullary broaching and stripping of the femur at the outer side to allow for segmental defect reconstruction have a dramatic effect on the vascularity of the femur. Stripping of the periosteum especially seemed to have a destructive effect on the regeneration process. Results of histologic examination in human retrievals with an intact femur are unknown.

The technique used for segmental defect reconstruction had an effect on the initial host response in the first weeks after surgery. The total amount of tissue ingrowth was smaller after defect reconstruction with a cortical strut in comparison with an open wire mesh after 6 weeks followup. A decreased rate of revascularization may have an effect on the rate of incorporation of the impacted grafts in the long term. Some authors doubt whether the incorporation process of impacted bone grafts is needed for a satisfying long-term clinical outcome and claim that complete incorporation might be associated with loosening of the implants.1,14 However, we think that incorporation of impacted bone grafts is an important factor in the long-term clinical outcome.26 In our clinic, successful outcome of acetabular reconstructions28 was associated with almost complete incorporation of the bone grafts.33

On the basis of a bone conduction chamber study, Tägil and Aspenberg30 suggested that a composite of bone cement and necrotic nonrevascularized grafts strengthened by fibrous ingrowth from the host may uphold mechanical strength in the first period after surgery when different stages of graft healing are present. It is debatable whether the mechanical strength of such a composite will remain strong enough to withstand forces in the long term. Therefore, complete incorporation of the grafts is needed. In our study, revascularization and fibrous ingrowth into the impacted grafts behind the strut and mesh were observed. The pattern of fibrous ingrowth and results from the microangiography were similar, indicating that invasion of blood vessels and fibrous tissue was a similar process. The technique used for segmental defect reconstruction had an effect on the revascularization pattern. A superficial zone of revascularized grafts with fibrous ingrowth was observed after defect reconstruction with a metal mesh. The presence of a structural graft hampered early invasion of the impacted graft by blood vessels and fibrous tissue. Only at the edges of the defect were revascularized areas seen, whereas medially behind the strut the impacted grafts were nonrevascularized in all cases. The absence of fibrous armoring may result in decreased stability in the early phase after surgery, after segmental defect reconstruction with a strut. On the medial side, this might lead to varus rotation and subsidence of the stem.

Regardless of the technique used for segmental defect reconstruction, the major complication in this animal study was a femoral periprosthetic fracture in 38% of the goats. In all femurs with a periprosthetic fracture, a healing response was seen near the fracture site. The proximal reconstruction was not harmed by the fractures and the histologic observations made in the femurs with fractures were similar to the histologic results in the femurs without fractures. Therefore, we think that the presence of a periprosthetic fracture did not influence graft revascularization in the proximal part of the femur. The high number of periprosthetic fractures can be explained partly by the critical-sized segmental defect that was created, which was as much as 70% of the length of the stem. In this study, three of seven (43%) reconstructions had a femoral fracture in the strut reconstruction group. Surprisingly, goats continued walking with weightbearing even on a fractured femur. Clinically no fracture was expected in any goat, except the one goat that was euthanized after a fall and was excluded from the results. Control radiographs only can be made with goats under general anesthesia and were not made regularly. The only observation in the goats with a femoral fracture at euthanasia was a progressive limp. Although a fall was responsible for two of the five fractures in this study, the reconstructed femur offered insufficient stability for full weightbearing in both groups. The combination of a necrotic cortex after surgery and a stress peak arising from the inserted stem in combination with the segmental defect probably played a major role. Furthermore, it is known that a temporary cortical bone weakness during creeping substitution starts approximately 3 weeks after necrosis.17 Because the exact time of the fractures was unknown, this might have played an additional role. In humans, a regimen of restricted loading should be used for a longer period, which was not possible in the goats. A long-stem prosthesis to provide for a better stability in cases with large defects can be used in humans.

Segmental defect reconstruction with a cortical strut graft significantly harms revascularization of the underlying impacted grafts. We recommend using an open wire mesh for segmental defect reconstruction in combination with impaction grafting of the femur to allow for optimal revascularization in an area with impaired vascularity. However, in some situations, depending on the type and extent of the bone defect in the patient, strut grafts are preferable for mechanical reasons. Regardless of the technique used for reconstruction, a regimen of restricted weightbearing and long-stem prostheses should be used in severely defective femurs.

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We thank Diny Versleijen and Leon Driessen for work on the histologic preparation.

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